Wheat-pea intercropping for aphid control: from laboratory tritrophic approach to field application | IJAAR Journals

Int. J. Agron. Agri. R.
Lopes et al. Page 20
RESEARCH PAPER OPEN ACCESS
Wheat-pea intercropping for aphid control: from laboratory
tritrophic approach to field application
Thomas Lopes*1
, Haibo Zhou2,3
, Julian Chen4
, Yong Liu5
, Bernard Bodson6
, Frédéric
Francis1
1
Functional and Evolutionary Entomology, Gembloux Agro-Bio Tech, University of Liege,
Gembloux, Belgium
2
Anhui Academy of Science and Technology, Heifei, PR China
3
Anhui Academy of Applied Technology, Heifei, PR China
4
State Key Laboratory for Biology of Plant Disease and Insect Pests, Institute of Plant Protection,
Chinese Academy of Agricultural Sciences, Beijing, PR China
5
College of Plant Protection, Shandong Agricultural University, Taian, PR China
6
Crop production, Gembloux Agro-Bio Tech, University of Liege, Gembloux, Belgium
Article published on September 15, 2016
Key words: Triticum aestivum, Pisum sativum, Aphididae, Biological control.
Abstract
Intercropping is an interesting practice to promote the sustainable control of insect pests such as aphids. In
particular, volatile organic compounds emitted by aphid-infested intercropped plants may deter other aphid
species from their host plants, while attracting natural enemies. In this study, olfactometer and net-cage
behavioural assays were first conducted to determine the effect of wheat-pea mixtures combined with aphid
infestations on odour preferences of the wheat aphid Sitobion avenae and two associated predator species, the
ladybird Harmonia axyridis and the hoverfly Episyrphus balteatus. Healthy wheat plants were preferred by S.
avenae, while wheat-pea mixtures combined with aphid infestations were significantly less attractive. H. axyridis
preferred odours from healthy wheat plants mixed with aphid-infested pea plants. As for E. balteatus, their
searching and oviposition behaviours were stimulated by the different wheat/pea combinations associated with
aphid infestations. A field trial was also carried to compare the effect of mix and strip cropping wheat with pea on
aphids and their natural enemies with both monocultures. Wheat and pea aphid populations were significantly
reduced by both types of intercropping when compared to monocultures. Moreover, higher abundances of
hoverflies, lacewings and ladybirds were found in wheat mixed with pea field, followed by strip cropping and
monocultures. These findings show that wheat-pea intercropping can be efficient to reduce aphid populations,
namely by promoting their biological control.
* Corresponding Author: Thomas Lopes  tlopes@doct.ulg.ac.be
International Journal of Agronomy and Agricultural Research (IJAAR)
ISSN: 2223-7054 (Print) 2225-3610 (Online)
http://www.innspub.net
Vol. 9, No. 3, p. 20-33, 2016

Introduction
Annual monoculture cropping systems greatly
simplified agroecosystems landscape structural
diversity, favouring the establishment of pest
populations (Andow, 1991; Landis and Marino, 1999).
In order to reduce the use of insecticides, which have
negative effects on human health (WHO, 1990) and
environment (Devine and Furlong, 2007), alternative
pest control methods have been developed, namely
based on habitat management practices (Gurr et al.,
2004; Hassanali et al., 2008). Among these,
intercropping, which is considered as the cultivation
of at least two plant species in the same place at the
same time (Andrews and Kassam, 1976; Ofori and
Stern, 1987; Anil et al., 1998), can be interesting for
the sustainable control of pests (Smith and McSorley,
2000; Hassanali et al., 2008; Konar et al., 2010;
Suresh et al., 2010; Vaiyapuri et al., 2010). Focusing
on pea (Pisum sativum Linnaeus)-wheat (Triticum
aestivum Linnaeus) intercropping systems, beneficial
effects were already observed on aphid control. In
fact, this practice can significantly decrease pea
aphid, Acyrthosiphon pisum (Harris) (Ndzana et al.,
2014; Lopes et al., 2015), and English grain aphid,
Sitobion avenae (Fabricius) (Zhou et al., 2009a;
Lopes et al., 2015), populations. However, the
mechanisms explaining how wheat-pea intercropping
promotes aphid control, which is called associational
resistance (Tahvanainen and Root, 1972), are not still
well understood (Ndzana et al., 2014).
The resource concentration hypothesis from Root
(1973) states that phytophagous insects are more
likely to find their host plants when those are
concentrated in dense or pure stands. Increasing
plant diversity by intercropping two or more plant
species may affect the visual and olfactory location of
herbivore’s host plants, as reviewed by Poveda et al.
(2008) and Barbosa et al. (2009). Focusing on
chemical cues, host plants location may be disrupted
when their odours are blended with neighboring non-
host plants. As shown by Xie et al. (2012), winged S.
avenae prefer wheat plant odours alone than blended
odours of wheat intercropped with mung bean (Vigna
radiate Linnaeus).
Moreover, herbivore-induced plant volatiles (HIPVs)
emitted by aphid-infested non-host intercropped
plants may deter other aphid species from their host
plants. It is namely the case with methyl salicylate
(MeSA), which can be emitted for example by aphid-
infested hops (Humulus lupulus Linnaeus) (Campbell
et al., 1993) and soybean (Glycine max (Linnaeus)
Merrill) (Zhu and Park, 2005) and repel cereal aphid
species (Pettersson et al., 1994). Moreover, HIPVs
such as MeSA may also attract aphid natural enemies
(Hatano et al., 2008), such as the ladybird Coccinella
septempunctata Linnaeus (Zhu and Park, 2005) and
the hoverfly Toxomerus marginatus (Say)
(Rodriguez-Saona et al., 2011). However, the effect of
HIPVs on aphids and their natural enemies has not
been studied in the context of wheat-pea
intercropping to our knowledge.
Therefore, the aim of this study was to determine the
behavioural preferences of S. avenae, an important
pest species that transmits efficiently the Barley
yellow dwarf virus (BYDV) to wheat (Gray et al.,
1998), when exposed to blended odours of pea plants
infested by the pea aphid, A. pisum, intercropped
with healthy or S. avenae infested wheat plants. The
same plant-aphid combinations were used to assess
the behavioural preferences of two important aphid
predator species, namely the multicolored Asian lady
beetle, Harmonia axyridis (Pallas), and the
marmalade hoverfly, Episyrphus balteatus DeGeer.
Complementarily, a field trial was conducted to assess
the effect of wheat-pea intercropping on aphids and
their natural enemies in real environmental
conditions.
Materials and methods
Plants and insects
Wheat (variety “Tybalt”) and pea (variety “James”)
were sown in plastic pots (9 × 8 × 10 cm). After plant
germination, S. avenae and A. pisum were
transeferred into wheat and pea respectively. Aphids
were moved to newly emerged plants each week to
guarantee their proper development.

H. axyridis adults were placed in aerated plastic
boxes containing sugar, water-impregnated cotton,
and multi-flower pollen. E. balteatus adults were
reared in cages (75 × 60 × 90 cm) containing bee-
collected pollen, sugar and water. Plants and insects
were kept in a climate-controlled room (16:8
light/dark; 22 ± 1 °C).
S. avenae and H. axyridis olfactometer behavioural
assays
A two-arm olfactometer similar to the one described
by Vet et al. (1983) was used to test S. avenae and H.
axyridis preferences for olfactory cues derived from
wheat-pea mixtures combined with aphid
infestations. The olfactometer was made entirely from
Teflon and was closed with a removable glass roof.
The walking arena was 40 cm wide (from center to
odor source) and 1.5 cm high (from Teflon walking
arena to glass ceiling). Charcoal-filtered air was
pushed in each of the olfactometer arms through
Teflon tubing and adjusted to 150 ml/min with a
digital flowmeter. A pump ventilated the walking
arena by removing air from the center at 300 ml/min.
A 1-l glass chamber (inner diameter: 10 cm; height:
145 cm) was connected to one of the olfactometer
arms and was used to dispose the odor source.
Eight dual choices were examined by comparing one
of the following odour sources to clean air: (1) 20
healthy wheat plants, (2) 20 healthy pea plants, (3)
20 aphid-infested wheat plants (infested with 50 S.
avenae 24 hours prior to the experiment), (4) 20
aphid-infested pea plants (infested with 50 A. pisum
24 hours prior to the experiment), (5) 20 healthy
wheat plants mixed with 20 healthy pea plants, (6) 20
aphid-infested wheat plants (same conditions as
above) mixed with 20 healthy pea plants, (7) 20
healthy wheat plants mixed with 20 aphid-infested
pea plants (same conditions as above), (8) 20 aphid-
infested wheat plants mixed with 20 aphid-infested
pea plants (same conditions as above for both).
Forty winged S. avenae were individually placed in
the center of the olfactometer. Their choise was
recorded when they crossed a “choice line”, which was
located 5 cm past the center of the walking arena, in
direction of each odour sources.
Aphids that did not cross a line within 10 min were
recorded as non-responders and excluded from
analysis. Concerning H. axyridis, 20 females were
individually randomly placed in the centre of the
olfactometer. Their choice was determined by the
time spent in each olfactometer zone. The duration of
repetitions was fixed at three minutes, which was
sufficient for individuals to explore the olfactometer
arena. Those who did not cross a line within three
minutes were considered as non-responders and
excluded from analysis. Each aphid and lady beetle
was tested only once. The olfactometer was cleaned
with norvanol after each repetition. Experiments were
conducted in a laboratory at 22 ± 1 °C and under
uniform lighting.
E. balteatus behavioural observations
Visual observations were conducted in a controlled
environment room (22 ± 1 °C). To do so, a net-cage
(180 × 60 × 90 cm) (Fig. 1.) was set up in a black box
(200 × 70 × 100 cm) consisting of a steel frame
covered with black cardboard paper to avoid external
visual cues. Uniform illumination was provided inside
the box by four fluorescent light tubes (70 W;
Luminux) positioned 10 cm above the net-cage.
Three pots containing wheat and pea plants were
placed in each side of the net-cage as presented in Fig.
1. E. balteatus females were collected from rearing
cages and individually placed in the center of the net-
cage. Their behaviour was then recorded during 10
min using the Observer® software (Noldus
information Technology, version 5.0, Wageningen,
The Netherlands). Five behavioural events were
observed as follows: (1) immobility: the hoverfly was
immobilized on the cage without moving, (2)
extensive flying: the hoverfly hovered in the cage far
away the plant, (3) searching: the hoverfly hovered in
the cage close to the plant, (4) acceptance: the
hoverfly landed on the plant, stayed immobile or
walked on it, with proboscis extension on the plant
surface, (5) oviposition: the hoverfly female showed
abdomen bending and laid eggs. Then individuals
were tested for each treatment.

Twelve series of dual-choice experiments were
compared (Table 1). The net cage was cleaned with
norvanol after each test.
Field experimental design
To assess the effect of wheat-pea intercropping on
aphids and their natural enemies, a field study was
conducted in the experimental farm of Gembloux
Agro-Bio Tech, University of Liege, Namur Province
of Belgium (50º33”N, 4º42”E) in 2011.
The field trial consisted of four treatments: (1) wheat
mixed with pea (WMP), (2) alternate strips of wheat
and pea (SWP), (3) wheat monoculture (WM), (4) pea
monoculture (PM). Plots positioned within wheat
crops were settled by delimiting three distinct areas
(4m × 10m each) for each treatment (total of 12 plots)
(Fig. 2.). Wheat (variety “Tybalt”) monoculture was
planted in 20-cm-apart rows at a rate of 350 seeds
per m2 on 18 February 2011. Pea (variety “James”)
monoculture was planted in 50-cm-apart rows at a
rate of 80 seeds per m2 on 18 February in 2011. For
wheat mixed with pea, pea was planted between the
two rows of wheat at a rate of 35 seeds per m2. No
insecticide or herbicide was used in the whole
experimental area. Wheat and pea were maintained
with standard agronomic practices used in Europe.
Insect diversity and abundance monitoring
Yellow pan traps (Flora®, 27 cm diameter and 10 cm
depth), which are frequently used to attract and trap
insects (Laubertie et al., 2006), were attached to
fiberglass sticks and placed 10 cm above the surface of
plants. Traps were filled with water and a few drops of
detergent. A single trap was installed in the middle of
each investigated plot (total of three traps per
treatment). Traps were emptied and reset at 7-day
intervals between 4 May and 29 June. Insects were
collected and transferred to plastic 50-mL vials
containing 70% ethanol. Aphids and their natural
enemies were sorted and identified to the species
level in the laboratory according to the following keys:
Taylor (1981) for aphids, Roy et al. (2013) for
ladybirds; van Veen (2010) for hoverflies; San Martin
(2004) for lacewings. The number of individuals per
species was also recorded.
Visual observations on plants were also performed to
visually assess the diversity and abundance of aphids
on wheat tillers and pea plants. To do so, 20 tillers or
plants (both in intercropping treatments) were
randomly observed in each plot.
Statistical analysis
Observed frequencies related to the choice of S.
avenae and H. axyridis in olfactometer behavioural
assays were compared to corresponding theoretical
frequencies by using a χ2 goodness-of-fit test. A
Student’s t test was performed to compare the mean
frequencies of E. balteatus responses to wheat and
pea stimuli. For field experiments, a data sqrt (n + 1)
transformation was applied to stabilize the variance
before each test. The density of insect populations
was compared among treatments using a one-way
analysis of variance (ANOVA), followed by Tukey’s
honestly significant differences (HSD) test. All
statistical tests were performed using Minitab® 16.
Results
S. avenae and H. axyridis olfactometer behavioural
assays
A strong preference of winged S. avenae was observed
for healthy wheat (χ2 = 32.00, P<0.001) and pea (χ2 =
24.50, P<0.001) plants odours (Fig. 3.). However, S.
avenae were not significantly attracted by odours
from aphid-infested wheat plants and by aphid-
infested wheat plants combined with aphid-infested
pea plants. Significantly higher proportions of non-
responding individuals were observed when exposed
to odours from infested pea plants (χ2 = 18.00,
P<0.001), as well as with the other three
combinations: wheat and pea (χ2 = 24.50, P<0.001),
wheat infested with aphids and pea (χ2 = 4.50,
P<0.05), wheat and pea infested with aphids (χ2 =
12.50, P<0.001).
Proportionally, H. axyridis females spent
significantly more time on aphid-infested wheat plant
odours (χ2 = 7.50, P<0.01) when compared to the
clean air, while the opposite was observed when they
were exposed to healthy wheat plants (χ2 = 4.52,
P<0.05).

The propotion of individuals that were attacted by
odours from healthy wheat plants mixed with aphid-
infested pea plants was significantly higher when
compared to the clean air (χ2 = 4.49, P<0.05). No
significant differences were observed between the
other treatments and the clean air (Fig. 4.).
E. balteatus behavioural observations
The combination of WA, PW and WA induced high
frequencies of searching by E. balteatus females
compared to the combination of WW, WW and WW
(Student’s t-test: t = 2.29, P<0.05) (Fig. 5.).
There were significant difference in acceptance
frequencies of E. balteatus females as follow groups:
PA, PA, PA and WA, WA, WA (Student’s t-test: t =
2.42, P<0.05), WW, PW, WW and WW, WW, WW
(Student’s t-test: t = 2.22, P<0.05), WA, PA, WA and
WW, WW, WW (Student’s t-test: t = 2.43, P<0.05).
Table 1. The different model (combination) between wheat and pea.
Series A B
1 2 3 4 5 6
Test 1 PW PW PW WW WW WW
Test 2 PW PW PW WA WA WA
Test 3 PA PA PA WW WW WW
Test 4 PA PA PA WA WA WA
Test 5 WW PW WW WW WW WW
Test 6 WW PW WW WA WA WA
Test 7 WW PA WW WW WW WW
Test 8 WW PA WW WA WA WA
Test 9 WA PW WA WW WW WW
Test 10 WA PA WA WA WA WA
Test 11 WA PA WA WW WW WW
Test 12 WA PW WA WA WA WA
PW: one pot of pea without aphids, PA=one pot of pea infested with aphids(50 ints), WW=one pot of wheat
without aphids, WA=one pot of wheat infested with aphids(50 ints) A and B represent zone A and B respectively,
1,2,3,4,5 and 6 represent the number of site in net-cage.
Moreover, the oviposition frequencies related to the
pea plant infested by related aphid or not were higher
than the ones observed with wheat plants (Fig. 5.
Student’s t-test: t = 2.38, P<0.05).
Field experiments
Diversity and abundance of aphids
Among the recorded aphid species, M. dirhodum and
S. avenae were predominant on wheat, while A.
pisum was predominant on pea plants. The
abundance of A. pisum was far higher than the one
from cereal aphids in both visual observations and
traps (Fig. 6. and Table 2). The population dynamics
of M. dirhodum, S. avenae and A. pisum exhibited
the same trends.
Population densities of M. dirhodum, S. avenae and
A. pisum reached their peak in all treatments on June
15th, June 22nd and June
22nd, respectively.
According to visual observations, M. dirhodum was
significantly more abundant in WM than in SWP and
in WMP both on peak occurrence period and on the
whole experimental duration (peak: F2,6 = 37.90,
P<0.01; total: F2,6 = 20.44, P<0.01). Similarly, a
significant difference for M. dirhodum in traps was
also detected among treatments (peak: F2, 6 = 21.43,
P<0.01; total: F2, 6 = 30.43, P<0.01). Consistently
with the results of M. dirhodum, the abundance of S.
avenae on wheat plants was significantly

higher in WM than in SWP and WMP both on peak
occurrence period and on the whole experimental
duration (peak: F2,6 = 34.78, P<0.01; total: F2,6 =
27.15, P<0.01). Similar results were found for S.
avenae in yellow traps (peak: F2, 6 = 61.27, P<0.01;
total: F2, 6 = 51.52,
P<0.01).
In addition, according to both trapping and visual
observations, population densities of A. pisum were
significantly reduced by mixing and strip
intercropping wheat with pea (Fig. 5.). The
abundance of A. pisum was significantly lower in
SWP and WMP than in PM (trap peak: F2, 6 = 32.22,
P<0.01, total: F2, 6 = 38.00, P<0.01; observation
peak:, F2, 6 = 31.38, P<0.01; total: F2, 6 = 79.64,
P<0.01).
Table 2. Diversity and abundance of aphids and related beneficials recorded in yellow traps in different crop
systems.
Species Treatments
Wheat-pea mixing Wheat-pea
strips
Wheat
monoculture
Pea
monoculture
%a
Aphids
Metopolophium dirhodum (W.) 578 437 949 0 67.6
Sitobion avenae (F.) 89 43 276 0 14.0
Acyrthosiphon pisum H. 64 131 0 339 18.4
Total 731 611 1225 339
Relative abundance (%) 25.1 21.0 42.2 11.7
Ladybirds 10.83b
Coccinella 7-punctata L. 5 17 8 9 40.2
Harmonia axyridis (P.) 5 14 8 18 46.4
Propylea 14-punctata (L.) 0 2 0 0 2.1
Harmonia 4-punctata (P.) 2 0 0 0 2.1
Calvia 14-guttata (L.) 1 1 1 4 7.2
Hippodamia variegate (G.) 1 1 0 0 2.0
Total 14 35 17 31
Hoverflies 43.08 b
Episyrphus balteatus (D.) 88 112 69 56 84.2
Scaeva pyrastri (L.) 0 3 2 0 1.3
Sphaerophoria scripta (L.) 5 8 4 0 4.4
Melanostoma scalare (F.) 0 1 2 0 0.8
Metasyrphus corolla (F.) 8 15 4 9 9.3
Total 101 139 81 65
Lacewing fly 46.09 b
Chrysoperla carnea (S.) 115 142 74 82 100.0
Total predators 230 316 172 178
Relative predator abundance (%) 25.6 35.3 19.2 19.9
aRelative occurrence of each species by family
bRelative occurrence of each family in beneficial populations.
Diversity and abundance of aphid natural enemies
Lacewings were the main aphid natural enemies
trapped (46.1%), followed by hoverflies (43.1%) and
ladybirds (10.8%). C. carnea, E. balteatus and H.
axyridis were the predominant recorded species
(Table 2).
Lacewings reached their occurrence peak in all
treatments on June 15th. Their abundance in each
treatment was low before June 8th even if they were
significantly more abundant in SWP than in others
three treatments at that period (F3, 8 = 15.00,
P<0.05).

Taking into account the whole experimental duration,
lacewings were significantly more abundant in SWP
and WMP when compared to both monocultures (F3, 8
= 8.73, P<0.05
Fig. 1. Schematic net-cage used for E. balteatus behavioural assays in response to cues originating from wheat
and pea. 1, 2, 3, 4, 5 and 6 represented sites for plant container setting, 7 represented site where E. balteatus were
released, A: the combination of plants A, B: the combination of plants B.
The occurrence peak of hoverflies occurred from 22nd
to 29th of June. There was no significant difference
among treatments in population densities before this
period. After that, their abundance was significantly
higher in SWP and WMP when
compared to both monocultures (F3, 8 = 114.43,
P<0.05). Taking into account the whole experimental
duration, hoverflies were significantly more abundant
in SWP followed by WMP, WM and PM (F3, 8 = 11.74,
P<0.05).
Fig. 2. Experimental field set-up to assess different kinds of wheat and pea associations on aphid and related
beneficial abundance and diversity.

As for ladybirds, their abundance of was significantly
higher SWP and WMP when compared to both
monocultures when taking into account the whole
experimental duration, the (F3, 8 = 12.39, P<0.05).
Discussion
Behavioural assays
Semiochemical-mediated host selection has been
shown to occur in several insect species (De Moraes et
al., 2001; Han and Chen, 2002; Sema Gencer et al.,
2009; Verheggen et al., 2008).
In the case of aphids, volatile organic compounds
(VOCs) are important olfactory cues for them to
locate their host plants (Döring, 2014).
Our results show that winged S. avenae significantly
prefer odours from healthy wheat or pea plants alone
when compared to the ones from different wheat-pea
mixtures combined with aphid infestations.
Fig. 3. Odour source selection (relative proportion of individuals choosing each arm) by winged Sitobion avenae
to different healthy/aphid-infested wheat and/or pea associations. **P<0.01, *P<0.05, NS: not significant.
Similarly, it as been reported that odours from
uninfested maize seedlings were significantly more
attractive to the leafhopper, Cicadulina storey China
than odours from C. storeyi-infested seedlings
(Oluwafemi et al., 2011). When tested individually for
behavioural activity, VOCs from C. storeyi-infested
seedlings such as methyl salicylate, (E)-
caryophyllene, and (E)-β-farnesene were repellent for
C. storeyi. Other behavioural assays also revealed that
several VOCs are released from herbivore-induced
tobacco plants exclusively at night and are highly
repellent to female moths from the species Heliothis
virescens (Fabricius) (De Moraes et al., 2001). In our
assays, odours from the mixture of healthy wheat and
pea were also deterrent to S. avenae. Similarly, Xie et
al. (2012) showed that S. avenae prefer wheat plant
odours alone than blended odours of wheat
intercropped with mung bean.
Herbivore-induced plant volatiles are also important
foraging cues for predators (Dicke et al., 1990). E.
balteatus foraging and reproductive behaviours are
known to be enhanced by volatiles emitted from
aphid-infested plants (Harmel et al., 2007). For
example, (Z)-3-hexenol and (E)-β-farnesene can
induce higher frequencies of E. balteatus female
searching and acceptance behaviour (Alhmedi et al.,
2010; Almohamad et al., 2008). Similar results were
obtained in our study as volatiles from wheat-pea
mixtures combined with aphid infestations were more
attractive for E. balteatus females, increasing their
frequencies of acceptance and oviposition.
Surprisingly, no significant attraction was found for
H. axyridis females, excepting when healthy wheat
was combined with aphid-infested pea.

For example, olfactometer experiments showed that
adult C. septempunctata were significantly more
attracted by odours from barley mixed with the
common weeds Cirsium arvense (Linnaeus) Scop.
and Elytrigia repens (Linnaeus) Nevski. than barley
alone (Ninkovic and Pettersson, 2003; Pettersson et
al., 2005). Similarly, Glinwood et al. (2009) reported
that C. septempunctata were more attracted to
combined odours from certain barley cultivars than
each cultivar alone. In another study, C.
septempunctata responded positively to volatiles
from aphid-infested barley plants and from
previously aphid-infested plants but not to volatiles
from uninfested plants (Ninkovic et al., 2001).
Despite our results, this suggests that olfactory cues
from diversified plant stands can be important
mechanisms in predator attraction to sites with a
complex botanical diversity.
Fig. 4. Odour source selection (relative proportion of individuals spending more time in the olfactomter arms) by
Harmonia axyridis females in response to to different healthy/aphid-infested wheat and/or pea associations in
dual-choice experiments. **P<0.01, *P<0.05, NS: not significant.
Fig. 5. Heatmap to illustrate behavioural changes (flying, landing and ovipositing on plants) of Episyrphus
balteatus females in relation to different dual choice experiments including healthy or aphid-infested wheat
and/or pea. Yellow to red colors correspond to increasing mean durations for hoverfly related activities.

Field trial
The aim of field habitat management is to create
suitable ecological infrastructures within the
agricultural landscape to decrease pest pressure on
crops and provide resources for natural enemies such
as alternative prey or hosts and shelter (Landis et al.,
2000). According to Root's natural enemies
hypothesis, generalist and specialist natural enemies
are expected to be more abundant in polycultures and
therefore suppress herbivore population densities
more in polycultures than in monocultures (Root,
1973). In our study, the abundance of lacewings,
hoverflies and ladybirds was
improved when pea was associated to wheat. This
could partly explain why the populations of cereal and
pea aphids were both decreased significantly when
compared to monocultures. Other factors such as the
physical obstruction (Perrin and Phillips, 1978) and
visual camouflage (Smith, 1969, 1976) of host plants
may have contributed to reduce the abundance of
aphids in wheat-pea associations. Other similar
studies showed that growing pea between rows of
wheat can reduce the populations of S. avenae and
enhanced those from natural enemies (Zhou et al.,
2009a; Zhou et al., 2009b).
Fig. 6. Abundance of aphids (Mean±SEM) recorded by visual observation in the different treatments during the
whole sampling period. Different letters indicate significant differences at P<0.05.
Overall, the above findings suggest that intercropping
plant species as an habitat management strategy can
be interesting to reduce aphid populations and
increase aphidophagous beneficials. The combination
of wheat and pea, with or without related aphid
species, improved the frequencies of acceptance and
oviposition by E. balteatus females, and also reduced
the attraction of S. avenae. Further behavioural
studies could focus on other important
aphidophagous such as lacewings and aphid
parasitoids. Results from our behavioural assays were
consistent with those from the field trial, supporting
the idea that wheat-pea associations are an efficient
tool for aphid biological control.
Therefore, it could be seen as an alternative method
to reduce the reliance on insecticides in
agroecosystems.
Acknowledgement
Thomas Lopes and Haibo Zhou have equally
contributed to this work. This research was supported
by grants from the Cooperation Project between
Belgium and China (CUDPICShandong,
2010DFA32810), the Anhui provincial natural science
foundation (1608085QC61), the Anhui postdoctoral
fund project for scientific and research, the Belgian
National Fund for Scientific Research (FNRS) which

provides a FRIA (Fund for Research in Industry and
Agronomy) PhD scholarship to Thomas Lopes, the
Ningxia Key Technology Research and Development
Program, and the Scientific Research Staring
Foundation for the Returned Overseas Chinese
Scholars, Ministry of Human Resources and Social
Security of the People's Republic of China.
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